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428 



J. Am. Mosq. Control Assoc. 



Vol. 1, No. 4 



LABORATORY BIONOMICS OF TRIPTEROIDES ARANOIDES 

TAKAO OKAZAWAS MASAHIRO HORIO^ MOTOYOSHl MOGP, ICHIRO MIYAGP 

AND SUPAT SUCHARIT" 

ABSTRACT. Tripteroides aranoides was colonized in the laboratory. Total duration of the immature stages 
was ca. 3 weeks at 28°C, L:D = 15.5:8.5 with an ample food supply. Retardation of 4th instar development was 
observed in larvae fed on insufficient food. Females were autogenous for the first clutch of eggs and required a 
blood meal for maturation of the second clutch. Mating was initiated in flight and copulation occurred on the 
cage wall. Gravid females hovered in small oblique loops above water in bamboo cups, whereupon a white egg 
appeared at the abdominal tip, which was propelled by the swing of the abdomen towards water surface. The 
females propelled eggs in the same manner into small apertures (11x4 mm) bored in bamboo. 



INTRODUCTION 

Tripteroides is one of the largest genera of the 
tribe Sabethini but the biology and behavior of 
the species in this genus have scarcely been 
studied. Miyagi (1973) observed the durations 
of the developmental stages and ovipositional 
behavior of Tp. bambusa (Yamada) in the labo- 
ratory. Mori (1976) described autogeny in this 
species. Beaver (1979) made observadons on 
the biology of 3 Tripteroides species in pitcher 
plants. For the rest of this genus, bionomic in- 
formation is virtually confined to descriptions 
of the breeding sites and observations on the 
attraction to humans at the time of collection 
(Mattingly 1981). 

In this study we established a laboratory col- 
ony of Tp. aranoides (Theobald) and observed 
the length of the developmental stages, blood- 
feeding, fecundity and mating and oviposi- 
tional behavior. 

MATERIALS AND METHODS 

Colony maintenance. The laboratory colony 
wras established with ca. 60 larvae collected from 
bamboo stumps in San Pa-Tong, south of 
Chiang Mai, Thailand. Gravid females were 
provided with a bamboo cup (ca. 10 cm diam 
and ca. 8 cm height) containing 200 ml tap 
water for oviposition. Hatched larvae were 
transferred to a white plastic tray (20 x 30 x 5 
cm) containing 1,000 ml tap water, and pow- 
dered mouse pellets plus dry yeast. Adults were 
maintained in screened cages (20 X 20 X 30 cm) 
and provided with cotton balls soaked with a 2% 



' Division of Parasitology, Department of Mi- 
crobiology, Saga Medical School. Nabeshima, Saga 
840-01, Japan. 

^ Department of Medical Zoology, School of 
Medicine, University of Occupational and Envi- 
ronmental Health, Kitakyusha 807, Japan. 

^ Laboratory of Medical Zoology, School of Health 
Sciences, Faculty of Medicine, University of the 
Ryukyus. Nishiharamachi, Okinawa 903-01, Japan, 

* Dept. of Medical Entomology, Faculty of Tropi- 
cal Medicine, Mahidol University, Bangkok I04()0, 
Thailand. 



sugar solution. The colony was maintained and 
the following observations made in an insectary 
at 28»C, 75-85% RH and L:D= 15.5:8.5, unless 
otherwise stated. 

Length of the developmental stages and 
REPRODUCTIVE PHYSIOLOGY. Three hundred 
larvae per tray were reared under 2 different 
conditions: one group was given 0.02 gm/day/ 
tray of food throughout larval life, the other 0.2 
gm before and 0.5 gm/day/tray after the ap- 
pearance of 4th instar larvae. The number and 
stage of larvae were recorded daily and pupae 
were checked for adult emergence. For larvae, 
the median time for development was deter- 
mined graphically from the 50% molting time. 
Cumulative percentages of stages from egg to 
pupa were plotted on graph paper daily. Points 
of each developmental stage were connected 
and the point at which the line crossed the 50% 
level indicated 50% molting time. One half of 
the adults emerging from each tray were given 
a 5% sugar solution and the other half, a 0.1% 
sugar solution. Females were dissected and ex- 
amined for mature eggs 6 days after 
emergence. 

Premating period for females was deter- 
mined from insemination rates. Ten to 20 
newly-emerged, 24, 48 or 72 hr-old females 
were kept in the 20 X 20 x 30 cm cages for 24 
hr with the same number of mature males. All 
females were dissected and their spermathecae 
were examined for insemination. The insemi- 
nation ability of males was determined from 
insemination rates of mature females kept for 
24 hr with newly-emerged, 24- or 48 hr-old 
males. 

The prefeeding periods of two groups of fe- 
males were determined by the incidence of en- 
gorgement among females offered a hairless 
mouse for 1 hour every day after emergence. 
One group was provided with a bamboo 
oviposition cup soon after emergence, white the 
other 3 weeks afterwards. 

To examine the possibility of maturing a sec- 
ond egg clutch without a blood meal, females 
fed on an ample food diet during larval life 
were allowed to lay eggs of the first clutch in a 
bamboo cup. All the eggs laid were removed 



December, 1985 



J. Am. Mosq. Control Assoc. 



429 



and counted daily. Five days after the last eggs 
were laid, parous females were divided into two 
groups. Females which engorged on a hairless 
mouse were provided access to a 0.1% sugar 
solution. The other, a blood-starved group, was 
given a 5% sugar solution. Six days later, all 
females were dissected to examine their ovaries. 

Egg resistance to desiccation. About 
2,000 eggs laid on the same day were collected 
on a filter paper and divided into 10 batches of 
152-292 eggs. One control batch was immedi- 
ately transferred to tap water and kept at SS'C 
and L;D= 15.5:8.5. Nine experimental batches 
were taken out of water 3 days after oviposition 
and held for storage at 20°C, 80% RH and 
L:D=12:12 for 4-50 days. Each batch was 
transferred to tap water at a scheduled time and 
larval hatch was examined daily for 35 days. 
Unhatched eggs were dissected to confirm the 
embryonic death. The hatch rate of the ex- 
perimental batches was corrected by that of the 
control. 

Mating and ovipositional behavior. Mat- 
ing and ovipositional behavior was observed in 
a screened cage or a glass box (20 x 20 x 30 
cm). Some observations were facilitated with 
close-up photographs. 

RESULTS 

Length of the developomental stages. The 
duration of each developmental stage under 
two different food regimens is presented in 
Table 1 . The mean duration time from oviposi- 
tion to adult emergence under an ample food 
supply was ca. 3 weeks. The duration time for 
males was a littie shorter than that for females. 
The total length of the larval stage under the 
insufficient food regimen was greaUy increased, 
due mainly to retarded growth at the 4th instar. 



Females required 20 days more than males for 
development. 

Reproductive physiology. Some males 
transferred sperm less then 24 hr after 
emergence (Fig. 1). Females were refractory to 
insemination 24 hr after emergence. Some were 
inseminated during 24-48 hr after emergence, 
and most all by 72 hr. Inseminated females 
appeared to be refractory to subsequent copu- 
lations. 

Females could produce first clutch eggs to 
maturity without a blood meal (Table 2). The 
autogeny rate was higher, and the mean 
number of matured eggs greater for females 
fed on ample food during both larval and adult 
stages than for those given insufficient food as 
larvae or adults. When underfed during both 
larval and adult stages, most females did not 
produce mature eggs. 

Rates of autogeny and numbers of mature 
eggs were related to wing length (Fig. 2). Fe- 
males with wing lengths less than 2.1 mm never 
produced mature eggs. All females with wings 
more than 2.6 mm long had mature eggs. Be- 
tween these extremes the rate of autogeny and 
number of mature eggs was positively corre- 
lated with wing length. The average fecundity 
(K) is given by the following equations: 

Y =RZ = 202.9 IX» - 1170.82X^ 
+ 2253. 33X - 1446.84 
R = 1.69X - 3.43 
Z = 119.92X2 

-448.66X + 421.45 

where R is rate of autogenous females, Z is 
number of mature eggs for autogenous females 
and X is wing length. 

Oviposition of the autogenous first clutch 
began 4 days after emergence and lasted for ca. 



Table 1. Duration of developmental stages and mortality of Tripteroides aranoides under two nutritional 

regimes. 







0.2/0.5* 




0.02 








(g/day/tray) 




(g/day/tray) 




Duration Mortality 


Duration 


Mortality 


Stage 




(days) 


(%) 


(days) 


(%) 


Egg 




4.2 (4-12)** 




4.2 (4-12) 




Larva*** 


I 


2.9 


1.3 


2.9 


2.7 




II 


1.5 


0.3 


2.2 


3.8 




III 


2.1 


0.3 


3.2 


5.0 




IV 


5.4 


1.4 


30.9 


1.1 


Pupa 


s 


4.9 (4-6) 


I 7. 


4.9 (4-6) 


7.6 




9 


5.0 (4-6) 




5.0 (4-6) 




Total 


S 


16.2 (14-19) 


4 9 


37.6 (15-68) 


18.7 


(Larva + Pupa) 


9 


17.9 (15-24) 




58.1 (20-85) 





* Larvae were fed on 0.2 g before and 0.5 g after appearance of 4th instar. 
** Ranges in parentheses. 
*** Obtained by graphic method. 



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J. Am. Mosq. Control Assoc. 



Vol. I, No. 4 




24 48 72 96 

TIME AFTER EMERGENCE (hOUR) 

Fig. 1. Time required for insemination of Trip- 
teroides aranoides. Ten to 20 females were dissected at 
each point. 



12 days (Fig. 3); that of the anautogenous sec- 
ond clutch began 4 days after engorgement. 
Females differed in their egg laying patterns: 
some laid the majority of the clutch in one day, 
while others laid small egg batches on different 
days. 

Blood feeding activity started after the be- 
ginning of oviposition. Females provided with a 
bamboo oviposition cup upon emergence took 
the first blood meal 6 days after emergence or 2 
days after the first oviposition. More than 95% 
of them took a blood meal within 15 days (Fig. 
4a). Females not provided with an oviposition 
cup rarely consumed blood before oviposition 
(Fig. 4b). Dissection of females soon after taking 
a blood meal revealed many mature eggs, which 
indicates that even partial oviposition can re- 
lease the blood feeding activity. 

A blood meal was required for the matura- 
tion of the second clutch of eggs. All 25 females 
which consumed blood had mature eggs. The 



Z = 119.92 X - <UI8.66 X + 421. «5 



r > 0.579 



' t 



'X:-' 




R . 1.69 X - 3.43 

r^ - 0.904 
(2.08 < X < 2.60) 



1.8 2.0 2.2 2.4 2.6 

WING LENGTH (MM) 

Fig. 2. Autogenous fecundity of Tripteroides 
aranoides in relation to wing length. Adults were fed 
on 5% sugar solution, a. Number of mature eggs 
(only females with mature eggs), b. Rate of females 
with mature eggs. 



mean number of mature eggs was greater for 
the anautogenous clutch (108.1 eggs) than for 
the preceding autogenous clutch (63.7 eggs). 
Without a blood meal, follicular development 
for the second clutch stopped at lib or earlier 
stages of Macan's system (1950) in 14 of 16 
blood-starved females. The remaining 2 had a 
small number of mature eggs (1 and 17 eggs). It 
was uncertain whether those were eggs of the 
second autogenous clutch or remnants of the 
first. 

Egg reslstance to desiccation. Soon after 
being laid, eggs could not be stored at 20°C and 



Table 2. Effects of larval and adult nutrition on the expression of autogeny in Tripteroides aranoides. 



Larval diet 

(g/day/tray) 


Sugar 

solution 

for adults 

(%) 




No. 


females 


No. mature 

eggs** 


lst-3rd 


4th 


Dissected 




Autogenous (%*) 


Mean* 




Range 


0.2 
0.02 


0.5 
0,02 


5 

0.1 

5 

0.1 


61 

51 
72 
35 




57 (93.4a) 

24 (47.1b) 

33 (45.8b) 

3 (8.6c) 


65.7a 
35.0b 
32.4b 
25.3b 




28-98 

7-63 

13-59 

17-36 



* Percentages and means followed by the different letters were significantly different by x'^-test (per- 
centages) or f-test (means) (P<0.01). 
** For autogenous females. 



December, 1985 



J. Am. Mosq. Control Assoc. 



431 




10 15 

DAYS AFTER EMERGENCE 



10 15 20 

DAYS AFTER ENGORGEMENT 



Fig. 3. Egg laying of Tripteroides aranoides females individually maintained. Arrows indicate blood-feeding. 



80% RH as all the eggs caved-in within a day. 
Three days after being laid, eggs retained the 
original shape after drying, but the percentage 
of flattened eggs increased with time. The 
hatching rate was above 70% for the first 16 
days of preservation, and decreased sharply 
thereafter (Fig. 5). A few eggs hatched after 35 
days of drying, but none hatched after 40 days. 
Mating behavior. Mating was initiated while 
both sexes were in flight. A male dashed to a 
flying female and caught her legs. Then the 
male slid under the body of the flying female 
and faced her. The couple flew to the cage wall 
or to the floor and rested. As soon as connect- 
ing his terminalia to that of the female, the male 
released his grasp and turned his body down; 
their bodies were then arranged in a straight 




b 




.[ 


/, 


1 L,. 



DAYS AFTER EfCRGENCE 



line, with heads in opposite directions (Fig. 6a). 
Turning of the male was sometimes finished 
before reaching the cage wall or floor. In such 
cases, both sexes beat their wings, but the 
couple flew in the direction of the female. 
Copulation continued for an average of 134.3 
seconds (range 106-165, n=15) after joining 
terminalia. The male beat his wings throughout 
the copulation. When the legs of a copulating 
male touched the cage floor, wing beating 
sometimes stopped. Males often hovered above 
bamboo cups awaiting females coming for 
oviposition. 



Fig. 4. Cumulative percentage of Tripteroides 
aranoides females taking a blood meal. a. Females 
given an oviposition cup soon after emergence, b. 
Females given a cup 3 weeks after emergence. 
Number of females observed was 43 for a, and 31 for 
b. Bars show number of eggs laid per female. Arrows 
indicate when a bamboo oviposition cup was given. 




10 20 30 40 

DAYS OF PRESERVATION AFTER DRYING 



Fig. 5. Relation of hatching rate to duration of dry 
condition. Eggs were taken out of water 3 days after 
oviposition. Number of eggs observed was 152-292 
per point. 



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J. Am. Mosq. Control Assoc. 



Vol. 1, No. 4 



OviPosiTioNAL BEHAVIOR. Females oviposited 
in flight. When a dosed bamboo internode (12 
cm diam and 12 cm height) with a lateral aper- 
ture (11x4 mm) was offered, gravid females 
flew around the bamboo internode. A female 
slowly approached the aperture with her pro- 
boscis directed downwards and antennae 
towards the aperture (Fig. 6b-ieft). In front of 
the aperture the female hovered in a small ob- 
lique loop several times, whereupon a single 
white egg appeared at the tip of the abdomen. 
Occasionally we observed females bearing 2 or 
3 eggs. Hovering still for a moment at a distance 
of 0.5— 1 cm from the aperture, the female 
swung her abdomen towards the target (Fig. 
6b-right). The egg was propelled 2.7-4.8 cm 
horizontally into the aperture. Unless the fe- 
male swung her abdomen, the egg remained 
attached to the tip of the abdomen. Sometimes 
females rested at the aperture with an egg on 
the tip of the abdomen, but we have never ob- 
served oviposition by females at rest on the 
bamboo, nor did females enter into the bamboo 
internode through the aperture. 

When an open bamboo cup was provided, 
gravid females hovered in oblique loops at a 
distance of 2- 10 cm from the water surface, 
whereupon an egg appeared. The female 
propelled the egg while swinging her abdomen 
towards the water surface. Some females faced 
the inside wall of the bamboo cup at a distance 
of 1-2 cm, and the projected eggs attached to 
the moist bamboo wall. 

In successive ovipositions, the female swung 
her abdomen once every 10-30 seconds. Since 
the number of the eggs laid in the bamboo cup 
was the same as that of the swinging modon, it is 



assumed that the female released an egg at each 
time of swinging. When a bamboo internode 
with an aperture was placed in the cage, the 
female laid an average of 4.6 eggs (range 1-31, 
nn = 98) in a single oviposition bout without 
rest or without flying to any other part of the 
cage from the oviposition site. 

DISCUSSION 

Reported lengths of immature stages in Trip- 
teroides are 5-6 weeks for Tp. aranoides, Tp. bam- 
husa and Tp. nepenthis (Edwards) collected from 
Nepenthes in Malaysia (Beaver 1979), 4-6 weeks 
for Tp. hisquamatus Lee (Assem 1959) and 20-29 
days for Tp. hamhusa (Yamada) (Miyagi 1973). 
These values were 1-2 weeks longer than the 
present observations for Tp. aranoides supplied 
ample food and reared at higher temperature. 
The different food conditions and tempera- 
tures may have produced different devel- 
opmental times. Inadequate food prolonged 
the larval stage in Tp. aranoides as in other mos- 
quitospecies(Moeurandlstock 1980, Mori 1979, 
Trpis 1979). Frank and Curtis (1977) found 
that delay in development of Wyeomyia larvae 
occurred principally in the 3rd instar under 
subopdmal nutrition. In Tp. aranoides the de- 
velopmental delay occurred mainly in the 4th 
instar. Such instar specificity of developmental 
delay has not been identified in the other Trip- 
teroides species. 

Some Tp. bambium females whose immature 
stages were reared at 15°C and 10 h photophase 
were autogenous, but at a higher temperature 
and longer photophase, autogeny was inhibited 
(Mori 1976). In contrast the rate of autogeny in 




Fig. 6. Behavior of Tripleroides aranoides. a. Copulation. Upper mosquito is female and lower male. b. Oviposi- 
tion into the aperture. Left female in approach and right in oviposition. 



December, 1985 



J. Am. Mosq. Control Assoc. 



433 



Tp. aranoides was very high, even under higher 
temperature (28°C) and longer photophase 
(15.5 h). This species may be autogenous for 
the first egg clutch under natural conditions in 
Thailand. 

I stock et al. (1975) reported an effect of food 
level on egg production in Wyeomyia smithii 
Coquillett. The number of eggs produced is 
greater for females fed on adequate food dur- 
ing the larval stage than for those fed on a 
limited quantity of food. Insufficient food at 
the adult stage reduced the autogeny rate and 
the egg number in Wyeomyia vanduzeei Dyar and 
Knab (Nayar et al. 1979). Insufficient food 
during the larval and/or adult stages affects the 
autogeny rate and the number of eggs pro- 
duced by Tp. aranoides. This means that the 
carbohydrates which Tp. aranoides adults take 
can be diverted to oogenesis, or that adults 
consume nutrients stored during larval life. 

In the Chiang Mai area the dry season con- 
tinues for ca. 6 months (November-April), 
during which bamboo stumps (the main 
breeding site for Tp. aranoides) seem to dry up. 
Tripteroides aranoides was found only in the rainy 
season in Burma Qolly 1933) and Yunnan 
(Chow 1949). Mattingly (1981) therefore in- 
ferred that this species passes over the dry sea- 
son in the adult or egg stage. Macdonald (1957) 
reported the eggs of Tp. aranoides resistant to 
desiccation for at least 10 days. In our study, 
eggs could not withstand desiccation over 40 
days under 80% RH, which is 20% higher than 
the mean humidity in March and April at 
Chiang Mai. We assume that Tp. aranoides con- 
tinues to breed in concealed habitats such as 
bored bamboos, in which sap accumulates even 
in the dry season, rather than pass the dry sea- 
son in the egg stage. 

In the mating behavior of Tp. aranoides, two 
successive steps were recognized; 1) contacting 
terminalia face to face, and 2) copula with heads 
in opposite directions. Mosquitoes with a short 
duration of mating, e.g., Aedes aegypti (Linn.) 
(Gwadz et al. 1971), usually complete insemina- 
tion at the former step, the latter being absent. 
Mosquitoes with a long duration, e.g., Aedes 
iriomotensis Tanaka and Mizusawa (Miyagi and 
Toma 1981), require the latter step for insemi- 
nation. 

The ovipositional behavior of Tp. aranoides is 
similar to that of Sabethes chloropterus Humboldt 
observed by Galindo (1958). Both species 
oviposit in small vertical holes while flying. 

Compared with the clutch size, the number of 
eggs laid by Tp. aranoides females in a single 
oviposition bout was fairly small. And females 
often lay eggs of a clutch on different days. This 
suggests that Tp. aranoides females deposit eggs 
in small batches at several different breeding 



places. Such low numbers of eggs in egg batches 
may decrease competition among offspring 
under limited food supply in small water col- 
lections surfi as bamboo internodes. 

ACKNOWLEDGMENTS 

We wish to express our gratitude to Prof. C. 
Khamboonruang, Chiang Mai University, for 
facilitating our research in Chiang Mai, Mr. T. 
Deesin, Mahidol University, Mr. W. Choochote, 
Chiang Mai University, Drs. M. Tsukamoto and 
T. Toma, members of the overseas research 
team, for their cooperation in collecting the 
material, and to Prof. K. Tokaichi, Saga Medi- 
cal School, for improving the English of die 
manuscript. We also thank Ms. K. Noda, Saga 
Medical School, for help in maintaining the col- 
ony. 

This study was supported by Grant-in-Aid 
for Overseas Scientific Survey (No. 58041058), 
the Ministry of Education, Sciences and Culture 
of Japan (Leader, Prof. I. Miyagi). 

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